Abstract
In this article we first point at the expansion of associative cortical areas in primates, as well as at the intrinsic changes in the structure of the cortical column. There is a huge increase in proportion of glutamatergic cortical projecting neurons located in the upper cortical layers (II/III). Inside this group, a novel class of associative neurons becomes recognized for its growing necessity in both inter-areal and intra-areal columnar integration. Equally important to the changes in glutamatergic population, we found that literature data suggest a 50% increase in the proportion of neocortical GABAergic neurons between primates and rodents. This seems to be a result of increase in proportion of calretinin interneurons in layers II/III, population which in associative areas represents 15% of all neurons forming those layers. Evaluating data about functional properties of their connectivity we hypothesize that such an increase in proportion of calretinin interneurons might lead to supra-linear growth in memory capacity of the associative neocortical network. An open question is whether there are some new calretinin interneuron subtypes, which might substantially change micro-circuitry structure of the primate cerebral cortex.
INTRODUCTION
The main biological substrate for mammalian mental abilities is the neuronal circuitry of the cerebral cortex. Tremendous evolutionary increase in the neuron number and cortical connections (; ) allowed humans to adopt language and mathematical skills, to make affective modulation of emotional cues, possess self-conceptualization, mentalization, as well as to have high capacity of cognitive flexibility and working memory (Rakic, 2009). Such complex functioning is strongly related to distinct expansion of multimodal – high order associative areas, particularly the granular areas of the frontal lobe (i.e., associative prefrontal cortex; Teffer and Semendeferi, 2012). These areas have no clear correlate in mice and rats (Uylings and van Eden, 1990). In addition to expansion in size, there are significant changes in intrinsic organization of cortical circuitries (Figure 1). There are novel neuronal elements that appear in the human cerebral cortex making organization of microcircuitry (and consequently functional properties) substantially different when compared to non-primate mammals ().
FIGURE 1
In this article we first give a short overview of evolutionary changes in the connectivity of a specific class of principal (glutamatergic) cortico-cortical projecting neurons, as well as a possible functional significance of those changes regarding increase in cognitive capabilities. We also found that present comparative anatomical data suggest a distinct role in reorganization of cortical microcircuitry for one of the GABAergic local circuit neuron classes, the calretinin expressing neurons that in primates have much higher proportion. We propose a possible mechanism how calretinin neurons might contribute to reorganization of microcircuitry in the human associative cortex and how this might be related to an increase of cognitive capabilities.
MICROCIRCUITRY CHANGES IN THE PRIMATE PREFRONTAL CORTEX AND INCREASE IN PROPORTION OF CALRETININ NEURONS
It is well recognized that upper layer pyramids (; Shepherd, 2011; Teffer and Semendeferi, 2012) are cortico-cortical projecting neurons (; ). It is less recognized that in primates, large deep layer III pyramids are long distance cortico-cortical neurons which establish in parallel connections with several cortical areas (; Yeterian et al., 2012). Experimental studies in rhesus monkey show that they are key elements in the circuitry involved in working memory and other prefrontal cortex-dependent associative cognitive functions (Wang et al., 2006; Verduzco-Flores et al., 2009). Data from various psychiatric disorders showed that selective alteration of large layer III pyramidal cells correlates with a decline in higher cognitive functions (; Selemon et al., 2003; ; ; ; ; Teffer and Semendeferi, 2012; Selemon et al., 2013) and developmental studies found that prominence in size of neurons in the upper cortical layers and peak in synaptic number appear by the end of infancy, stage when human specific mental capacities appear (, ). Altogether, it can be concluded that large layer III pyramidal neurons in the high order associative areas are the main integrative elements (“associative” neurons) between different cortical areas (; see discussion from ).
Pyramidal neurons located in upper layers of the primate prefrontal cortex also provide rich intracortical projections. From large layer III pyramids 80% of synaptic output belongs to local connections coming from axonal side branches (). They extend several millimeters around, with dense columnar termination through layers II and III.
Human brain evolution is characterized by an increase in the number and width of minicolumns, but also in the increase of space available for interconnectivity between neurons, especially in the human prefrontal cortex where associative layer III pyramidal neurons are particularly abundant (; Spocter et al., 2012). Except to primary regions, prefrontal cortex established connections with all other cortical areas (). That way efficacy of inter- and intra-areal integration within prefrontal cortex correlates with overall level of information processing, influencing consequently level of individual cognitive capability (). Inter-individual differences in internal structure of upper cortical layers of human prefrontal cortex (Rajkowska and Goldman-Rakic, 1995a,b) make additional support that associative layer III neuron class has the major role in increasing the efficiency of cortico-cortical network (; ).
In parallel with evolutionary changes in connectivity of cortico-cortical network, significant changes appear in the organization of GABAergic network. This network acts as intrinsic modulator of cortical output since it is composed of local circuit neurons (interneurons; ). Numerous studies analyzing laminar distribution and density of cortical GABAergic neuron subpopulations were performed in various species (Table 1A). It is curious that only rarely the same group performed a systematic analysis of several species, using the same methodology, making it difficult to conclude about interspecies differences. Most of the studies performed in rat and mouse found that cortical GABAergic neurons represent around 15% (14–16%) of the overall population. In monkey and human their proportion mostly exceeds 20% (20–29%) suggesting an increase in proportion for about 30–50%.
Table 1
| (A) Percentage of GABAergic cells in the total neuron population | ||
|---|---|---|
| Anatomical area | Rat and mouse – GABA in total | Monkey and human – GABA in total |
| Primary visual area (V1) | 15% () – Rat | 20.5% () – Monkey |
| 14.5% () – Rat | 15% () – Monkey | |
| 15% () – Rat | 20% () – Monkey | |
| Primary somatic sensory area (S1) | 14% () – Rat | 20–29% () – S1 and primary motor area-Monkey |
| 25% (Ren et al., 1992) – Rat | ||
| Frontal lobe | 22% (Santana et al., 2004) – Rat | 24.9% ( – Monkey |
| 16% () – Rat | 21.2% () – Human | |
| Temporal lobe | 37.7% () – only layers II and III-Human | |
| Multiple lobe analysis | 19.5% (Tamamaki et al., 2003) – Mouse | 25% () |
| 15% () – Rat | ||
| (B) Percentage of calretinin expressing neurons within GABAergic population | ||
| Anatomical area | Rat and mouse – calretinin in GABA | Monkey and human – calretinin in GABA |
| Primary visual area (V1) | 17% () – Rat | 20% (Yan et al., 1995) – Monkey |
| 24% () – Mouse | ||
| Frontal lobe | 16.1% (Uematsu et al., 2008) – Rat | 28.6% (Zaitsev et al., 2005) – Monkey |
| 24.7%* () – Rat | 28.8%* – Human 34.2%* – Monkey (Sherwood et al., 2004) | |
| 18% () – Rat | 33.2–44.8%* (; ; )* – Monkey | |
| Temporal lobe | 46.2% () – only layers II and III-Human | |
| Multiple lobe analysis | 18% (Xu et al., 2010) – Mouse | |
| 13.9% (Tamamaki et al., 2003) – Mouse | ||
Overview of publications quantifying proportion of GABAergic and calretinin neurons in the neocortex of rodents and primates. (A) Proportion of GABAergic cells in population of all neurons, and (B) proportion of calretinin neurons inside the GABAergic population.
Values reported with an asterisk have been calculated from values presented in the original papers.
This large increase in proportion of GABAergic neurons seems to be principally caused by increase in number of neurons containing calretinin. Another two main classes, those containing parvalbumin and somatostatin, do not show such a robust increase in proportion (). In rodents the proportion of calretinin neurons among the total population of GABAergic neurons is between 16–18%, whereas in primate the proportion of calretinin reaches in some areas 35–40% (Table 1B). have estimated that, within layer II and III of associative temporal cortex in the human, GABAergic neurons represent around 1/3 of the total number of neurons, and almost half of GABAergic neurons express calretinin. In addition, a recent study () suggests that, in the human and monkey, calretinin neurons are two times more numerous in the frontal and parietal cortical areas. Collectively all these data indicate that the evolution lead to an increase in calretinin proportion in the upper cortical layers of high order associative regions. Our preliminary observations, comparing orbital frontal cortex in the rat and complementary area 14 in the rhesus monkey, showed a four- to fivefold increase in the proportion of calretinin for the upper cortical layers, where calretinin neurons cover almost 15% of the total number of neurons ().
FUNCTIONAL PROPERTIES OF CALRETININ NEURONS
For efficient functioning of the human cerebral cortex with its complex areal subdivision and increased number of cortical columns, there is a need for enhanced inter-areal and intra-areal integration (Sherwood et al., 2005; ). Appearance of most likely, evolutionary new associative neurons (; ; Spruston, 2008) makes substantial changes in the organization of microcircuitry and allows higher level of network integration (). Inside the primate cortico-cortical network there is also a fivefold increase in proportion of calretinin neurons and it is reasonable to ask how this changes the microcircuitry structure.
Based on electrophysiological properties, two main types of calretinin interneurons can be distinguished in rodents: accommodating and non-adapting non-fast spiking cells (; ; ). These electrophysiological features are correlated with expression of a group of membrane voltage gated proteins (), the calretinin cluster (Toledo-Rodriguez et al., 2004; Schwaller, 2014).
Different types of calretinin neurons can be identified based on their morphological features, particularly on the postsynaptic domain targeted by their axon. Double bouquet cells have vertically oriented axons which project mainly to basal dendrites of pyramidal cells (; Yanez et al., 2005), while bipolar () and bitufted cells () project to the proximal and middle region of pyramidal cell’s apical dendrite. Therefore, calretinin neurons provide direct inhibition, although with a low connectivity rate of ∼10% (), on mid-proximal dendritic domain of pyramidal cell (i.e., proximal parts of apical and basal dendrites). In addition to this sparse connectivity with nearby pyramids, calretinin neurons provide strong innervation onto somatostatin neurons (Pfeffer et al., 2013) and other calretinin cells (). These somatostatin neurons are known for providing direct inhibition of pyramidal cell’s apical and basal dendrites (Wang et al., 2004; ), as well as for providing an inhibitory influence on parvalbumin neurons (Pfeffer et al., 2013).
Parvalbumin neurons are mostly basket cells, which exert strong inhibitory control over pyramid’s soma (; Pfeffer et al., 2013). Optogenetic activation of fast spiking parvalbumin cells induces gamma oscillations in nearby pyramids () and, without parvalbumin activity, pyramids would continue to fire but without synchrony (). In other words, parvalbumin basket cells phase-lock their target pyramids through hyperpolarization, after which pyramids undergo rebound, but short lived depolarization and fire in synchrony (). Elimination of inhibitory influences on parvalbumin basket cells prolongs their influence on pyramids (Pouille and Scanziani, 2004), and this is where the potential role of calretinin neurons could reside. By inhibiting somatostatin neurons (Pfeffer et al., 2013; ) they could create a disinhibitory window for parvalbumin baskets. We hypothesize that this, by calretinin neurons provided disinhibition, might prolong the effect of parvalbumin cells on pyramids, allowing longer periods of synchronized gamma oscillations.
This group of cells, including calretinin neurons, their somatostatin targets, parvalbumin neurons, and their pyramidal targets, can be collectively called a neuronal assembly (; Somogyi et al., 2014). The significance of an assembly is that it can activate its efferent targets with high probability, through the synchronous activity of its pyramids (; ). Interneurons are needed to segregate, maintain and also establish a temporal sequence of activation between particular assemblies (Somogyi et al., 2014). We hypothesize that the role of increased proportion of calretinin neurons would depend on the criteria of their territorial exclusivity, i.e., their developmental positioning to efferent targets compared to other calretinin interneurons. If newly added calretinin cells show no territorial exclusivity, i.e., their connections significantly overlap with those of pre-existent calretinin neurons, they would be incorporated into already established assemblies, connecting to somatostatin neurons to which some calretinin neurons have previously connected. Hence, there would be an increased number of calretinin cells per assembly, while the number of pyramids would not change, allowing for a more potent overall effect of calretinin neurons. However, in case of the other extreme, newly added calretinin cells will mostly connect to their own group of pyramids and parvalbumin and somatostatin neurons, creating smaller assemblies and allowing for more parallel processing. More parallel units might lead to supra-linear growth in memory capacity of the neocortical network, which is of particular importance in regions involved in planning and executive functions.
Present evidence suggests that the evolutionary path of the primate cortico-cortical network seems to have been an expansion in two aspects. First, there is an increase in proportion of principal neurons located in layers II and III, which would be a way to create the basic excitatory architecture for inter-areal processing. Second, there is an increase in proportion of calretinin expressing GABAergic interneurons, which would be a way to create a gain in synchrony and parallel processing between disparate cortical areas. An open question is whether this jump in proportion of calretinin neurons is based on a simple expansion of already preexistent subtypes of these cells found in the rodents or do we have some new cellular subtypes. If so, this might produce a more profound changes then simple supra-linear increase in their number, similar to changes occurring with appearance of associative principal neurons. These two might have been converging processes, making structure of microcircuitry in the primate neocortex substantially different when compared to other non-primate mammals.
Statements
Acknowledgments
We wish to thank Dr. Monique Esclapez and Prof. Marijan Klarica for helpful comments and discussions on this manuscript. This work was supported by the University of Zagreb short term grant “Prolonged proliferation of cortical GABAergic neurons in primates” and Croatian Science Foundation grant “Microcircuitry of higher cognitive functions.”
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Summary
Keywords
GABA, calretinin, neocortex, pyramidal neurons, species differences
Citation
Džaja D, Hladnik A, Bičanić I, Baković M and Petanjek Z (2014) Neocortical calretinin neurons in primates: increase in proportion and microcircuitry structure. Front. Neuroanat. 8:103. doi: 10.3389/fnana.2014.00103
Received
01 May 2014
Accepted
07 September 2014
Published
25 September 2014
Volume
8 - 2014
Edited by
Nada Zecevic, University of Connecticut Health Center, USA
Reviewed by
Gundela Meyer, Universidad de La Laguna, Spain; Srdjan D. Antic, University of Connecticut Health Center, USA
Copyright
© 2014 Džaja, Hladnik, Bičanić, Baković and Petanjek.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Domagoj Džaja, Laboratory for Neuromorphometry, Department of Neuroscience, Croatian Institute for Brain Research, School of Medicine, University of Zagreb, Šalata 12,10000 Zagreb, Croatia e-mail: domagojdzaja@gmail.com
This article was submitted to the journal Frontiers in Neuroanatomy.
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